Abstract

Retinal imaging working with a line scan mechanism and a line camera has the potential to image the eye with a near-confocal performance at the high frame rate, but this regime has difficulty to collect sufficient imaging light while adequately digitize the optical resolution in adaptive optics imaging. To meet this challenge, we have developed an adaptive optics line scan ophthalmoscope with an anamorphic point spread function. The instrument uses a high-speed line camera to acquire the retinal image and act as a confocal gate. Meanwhile, it employs a digital micro-mirror device to modulate the imaging light into a line of point sources illuminating the retina. The anamorphic mechanism ensures adequate digitization of the optical resolution and increases light collecting efficiency. We demonstrate imaging of the living human retina with cellular level resolution at a frame rate of 200 frames/second (FPS) with a digitization of 512 × 512 pixels over a field of view of 1.2° × 1.2°. We have assessed cone photoreceptor structure in images acquired at 100, 200, and 800 FPS in 2 normal human subjects, and confirmed that retinal images acquired at high speed rendered macular cone mosaic with improved measurement repeatability.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (8)

L. Sawides, A. de Castro, and S. A. Burns, “The organization of the cone photoreceptor mosaic measured in the living human retina,” Vision Res. 132, 34–44 (2017).
[Crossref] [PubMed]

M. A. Wilk, A. M. Dubis, R. F. Cooper, P. Summerfelt, A. Dubra, and J. Carroll, “Assessing the spatial relationship between fixation and foveal specializations,” Vision Res. 132, 53–61 (2017).
[Crossref] [PubMed]

A. E. Elsner, T. Y. Chui, L. Feng, H. X. Song, J. A. Papay, and S. A. Burns, “Distribution differences of macular cones measured by AOSLO: Variation in slope from fovea to periphery more pronounced than differences in total cones,” Vision Res. 132, 62–68 (2017).
[Crossref] [PubMed]

P. Tanna, M. Kasilian, R. Strauss, J. Tee, A. Kalitzeos, S. Tarima, A. Visotcky, A. Dubra, J. Carroll, and M. Michaelides, “Reliability and Repeatability of Cone Density Measurements in Patients With Stargardt Disease and RPGR-Associated Retinopathy,” Invest. Ophthalmol. Vis. Sci. 58(9), 3608–3615 (2017).
[Crossref] [PubMed]

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

J. Lu, B. Gu, X. Wang, and Y. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref] [PubMed]

A. E. Salmon, R. F. Cooper, C. S. Langlo, A. Baghaie, A. Dubra, and J. Carroll, “An Automated Reference Frame Selection (ARFS) Algorithm for Cone Imaging with Adaptive Optics Scanning Light Ophthalmoscopy,” Transl. Vis. Sci. Technol. 6(2), 9 (2017).
[Crossref] [PubMed]

A. Duan, P. A. Bedggood, A. B. Metha, and B. V. Bui, “Reactivity in the human retinal microvasculature measured during acute gas breathing provocations,” Sci. Rep. 7(1), 2113 (2017).
[Crossref] [PubMed]

2016 (9)

A. Duan, P. A. Bedggood, B. V. Bui, and A. B. Metha, “Evidence of Flicker-Induced Functional Hyperaemia in the Smallest Vessels of the Human Retinal Blood Supply,” PLoS One 11(9), e0162621 (2016).
[Crossref] [PubMed]

A. de Castro, G. Huang, L. Sawides, T. Luo, and S. A. Burns, “Rapid high resolution imaging with a dual-channel scanning technique,” Opt. Lett. 41(8), 1881–1884 (2016).
[Crossref] [PubMed]

J. Lu, B. Gu, X. Wang, and Y. Zhang, “Adaptive optics parallel near-confocal scanning ophthalmoscopy,” Opt. Lett. 41(16), 3852–3855 (2016).
[Crossref] [PubMed]

R. F. Cooper, Y. N. Sulai, A. M. Dubis, T. Y. Chui, R. B. Rosen, M. Michaelides, A. Dubra, and J. Carroll, “Effects of Intraframe Distortion on Measures of Cone Mosaic Geometry from Adaptive Optics Scanning Light Ophthalmoscopy,” Transl. Vis. Sci. Technol. 5(1), 10 (2016).
[Crossref] [PubMed]

R. F. Cooper, M. A. Wilk, S. Tarima, and J. Carroll, “Evaluating Descriptive Metrics of the Human Cone Mosaic,” Invest. Ophthalmol. Vis. Sci. 57(7), 2992–3001 (2016).
[Crossref] [PubMed]

J. Lammer, S. G. Prager, M. C. Cheney, A. Ahmed, S. H. Radwan, S. A. Burns, P. S. Silva, and J. K. Sun, “Cone Photoreceptor Irregularity on Adaptive Optics Scanning Laser Ophthalmoscopy Correlates With Severity of Diabetic Retinopathy and Macular Edema,” Invest. Ophthalmol. Vis. Sci. 57(15), 6624–6632 (2016).
[Crossref] [PubMed]

J. I. Morgan, “The fundus photo has met its match: optical coherence tomography and adaptive optics ophthalmoscopy are here to stay,” Ophthalmic Physiol. Opt. 36(3), 218–239 (2016).
[Crossref] [PubMed]

M. Lombardo, M. Parravano, S. Serrao, L. Ziccardi, D. Giannini, and G. Lombardo, “Investigation of Adaptive Optics Imaging Biomarkers for Detecting Pathological Changes of the Cone Mosaic in Patients with Type 1 Diabetes Mellitus,” PLoS One 11(3), e0151380 (2016).
[Crossref] [PubMed]

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual Foveal Cone Structure in CNGB3-Associated Achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

2015 (5)

J. C. Horton, A. B. Parker, J. V. Botelho, and J. L. Duncan, “Spontaneous Regeneration of Human Photoreceptor Outer Segments,” Sci. Rep. 5(1), 12364 (2015).
[Crossref] [PubMed]

E. Y. Chew, T. E. Clemons, T. Peto, F. B. Sallo, A. Ingerman, W. Tao, L. Singerman, S. D. Schwartz, N. S. Peachey, and A. C. Bird, “Ciliary neurotrophic factor for macular telangiectasia type 2: results from a phase 1 safety trial,” Am. J. Ophthalmol. 159(4), 659–666 (2015).
[Crossref] [PubMed]

A. Roorda and J. L. Duncan, “Adaptive optics ophthalmoscopy,” Annu Rev Vis Sci 1(1), 19–50 (2015).
[Crossref] [PubMed]

Y. Yu, T. Zhang, A. Meadway, X. Wang, and Y. Zhang, “High-speed adaptive optics for imaging of the living human eye,” Opt. Express 23(18), 23035–23052 (2015).
[Crossref] [PubMed]

T. Zhang, P. Godara, E. R. Blanco, R. L. Griffin, X. Wang, C. A. Curcio, and Y. Zhang, “Variability in Human Cone Topography Assessed by Adaptive Optics Scanning Laser Ophthalmoscopy,” Am. J. Ophthalmol. 160(2), 290–300 (2015).
[Crossref] [PubMed]

2014 (4)

A. Meadway, X. Wang, C. A. Curcio, and Y. Zhang, “Microstructure of subretinal drusenoid deposits revealed by adaptive optics imaging,” Biomed. Opt. Express 5(3), 713–727 (2014).
[Crossref] [PubMed]

Y. Yu and Y. Zhang, “Dual-thread parallel control strategy for ophthalmic adaptive optics,” Chin. Opt. Lett. 12(12), 121202 (2014).
[Crossref] [PubMed]

M. N. Muthiah, C. Gias, F. K. Chen, J. Zhong, Z. McClelland, F. B. Sallo, T. Peto, P. J. Coffey, and L. da Cruz, “Cone photoreceptor definition on adaptive optics retinal imaging,” Br. J. Ophthalmol. 98(8), 1073–1079 (2014).
[Crossref] [PubMed]

B. S. Liu, S. Tarima, A. Visotcky, A. Pechauer, R. F. Cooper, L. Landsem, M. A. Wilk, P. Godara, V. Makhijani, Y. N. Sulai, N. Syed, G. Yasumura, A. K. Garg, M. E. Pennesi, B. J. Lujan, A. Dubra, J. L. Duncan, and J. Carroll, “The reliability of parafoveal cone density measurements,” Br. J. Ophthalmol. 98(8), 1126–1131 (2014).
[Crossref] [PubMed]

2013 (3)

J. Carroll, D. B. Kay, D. Scoles, A. Dubra, and M. Lombardo, “Adaptive optics retinal imaging--clinical opportunities and challenges,” Curr. Eye Res. 38(7), 709–721 (2013).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Optical imaging of human cone photoreceptors directly following the capture of light,” PLoS One 8(11), e79251 (2013).
[Crossref] [PubMed]

A. Meadway, C. A. Girkin, and Y. Zhang, “A dual-modal retinal imaging system with adaptive optics,” Opt. Express 21(24), 29792–29807 (2013).
[Crossref] [PubMed]

2012 (5)

F. Felberer, J. S. Kroisamer, C. K. Hitzenberger, and M. Pircher, “Lens based adaptive optics scanning laser ophthalmoscope,” Opt. Express 20(16), 17297–17310 (2012).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Direct visualization and characterization of erythrocyte flow in human retinal capillaries,” Biomed. Opt. Express 3(12), 3264–3277 (2012).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Variability in bleach kinetics and amount of photopigment between individual foveal cones,” Invest. Ophthalmol. Vis. Sci. 53(7), 3673–3681 (2012).
[Crossref] [PubMed]

R. Wen, W. Tao, Y. Li, and P. A. Sieving, “CNTF and retina,” Prog. Retin. Eye Res. 31(2), 136–151 (2012).
[Crossref] [PubMed]

C. L. Cepko, “Emerging gene therapies for retinal degenerations,” J. Neurosci. 32(19), 6415–6420 (2012).
[Crossref] [PubMed]

2011 (5)

K. E. Talcott, K. Ratnam, S. M. Sundquist, A. S. Lucero, B. J. Lujan, W. Tao, T. C. Porco, A. Roorda, and J. L. Duncan, “Longitudinal study of cone photoreceptors during retinal degeneration and in response to ciliary neurotrophic factor treatment,” Invest. Ophthalmol. Vis. Sci. 52(5), 2219–2226 (2011).
[Crossref] [PubMed]

D. R. Williams, “Imaging single cells in the living retina,” Vision Res. 51(13), 1379–1396 (2011).
[Crossref] [PubMed]

D. T. Miller, O. P. Kocaoglu, Q. Wang, and S. Lee, “Adaptive optics and the eye (super resolution OCT),” Eye (Lond.) 25(3), 321–330 (2011).
[Crossref] [PubMed]

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.) 25(3), 301–308 (2011).
[Crossref] [PubMed]

A. Dubra and Y. Sulai, “Reflective afocal broadband adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 2(6), 1757–1768 (2011).
[Crossref] [PubMed]

2010 (3)

A. Roorda, “Applications of adaptive optics scanning laser ophthalmoscopy,” Optom. Vis. Sci. 87(4), 260–268 (2010).
[PubMed]

P. Godara, A. M. Dubis, A. Roorda, J. L. Duncan, and J. Carroll, “Adaptive optics retinal imaging: emerging clinical applications,” Optom. Vis. Sci. 87(12), 930–941 (2010).
[Crossref] [PubMed]

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci. 51(3), 1691–1698 (2010).
[Crossref] [PubMed]

2009 (5)

2007 (3)

2006 (4)

2005 (2)

F. Romero-Borja, K. Venkateswaran, A. Roorda, and T. Hebert, “Optical slicing of human retinal tissue in vivo with the adaptive optics scanning laser ophthalmoscope,” Appl. Opt. 44(19), 4032–4040 (2005).
[Crossref] [PubMed]

Q. S. Hanley, K. A. Lidke, R. Heintzmann, D. J. Arndt-Jovin, and T. M. Jovin, “Fluorescence lifetime imaging in an optically sectioning programmable array microscope (PAM),” Cytometry A 67(2), 112–118 (2005).
[Crossref] [PubMed]

2004 (1)

S. Martinez-Conde, S. L. Macknik, and D. H. Hubel, “The role of fixational eye movements in visual perception,” Nat. Rev. Neurosci. 5(3), 229–240 (2004).
[Crossref] [PubMed]

2002 (1)

2001 (2)

1999 (1)

Q. S. Hanley, P. J. Verveer, M. J. Gemkow, D. Arndt-Jovin, and T. M. Jovin, “An optical sectioning programmable array microscope implemented with a digital micromirror device,” J. Microsc. 196(3), 317–331 (1999).
[Crossref] [PubMed]

1997 (1)

1993 (1)

C. A. Curcio, C. L. Millican, K. A. Allen, and R. E. Kalina, “Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina,” Invest. Ophthalmol. Vis. Sci. 34(12), 3278–3296 (1993).
[PubMed]

1990 (1)

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[Crossref] [PubMed]

1988 (1)

D. R. Williams, “Topography of the foveal cone mosaic in the living human eye,” Vision Res. 28(3), 433–454 (1988).
[Crossref] [PubMed]

1987 (1)

1983 (1)

D. R. Williams and R. Collier, “Consequences of spatial sampling by a human photoreceptor mosaic,” Science 221(4608), 385–387 (1983).
[Crossref] [PubMed]

1982 (1)

J. I. Yellott., “Spectral analysis of spatial sampling by photoreceptors: topological disorder prevents aliasing,” Vision Res. 22(9), 1205–1210 (1982).
[Crossref] [PubMed]

1977 (1)

A. S. French, A. W. Snyder, and D. G. Stavenga, “Image degradation by an irregular retinal mosaic,” Biol. Cybern. 27(4), 229–233 (1977).
[Crossref] [PubMed]

Ahmed, A.

J. Lammer, S. G. Prager, M. C. Cheney, A. Ahmed, S. H. Radwan, S. A. Burns, P. S. Silva, and J. K. Sun, “Cone Photoreceptor Irregularity on Adaptive Optics Scanning Laser Ophthalmoscopy Correlates With Severity of Diabetic Retinopathy and Macular Edema,” Invest. Ophthalmol. Vis. Sci. 57(15), 6624–6632 (2016).
[Crossref] [PubMed]

Allen, K. A.

C. A. Curcio, C. L. Millican, K. A. Allen, and R. E. Kalina, “Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina,” Invest. Ophthalmol. Vis. Sci. 34(12), 3278–3296 (1993).
[PubMed]

Arathorn, D. W.

Arndt-Jovin, D.

Q. S. Hanley, P. J. Verveer, M. J. Gemkow, D. Arndt-Jovin, and T. M. Jovin, “An optical sectioning programmable array microscope implemented with a digital micromirror device,” J. Microsc. 196(3), 317–331 (1999).
[Crossref] [PubMed]

Arndt-Jovin, D. J.

Q. S. Hanley, K. A. Lidke, R. Heintzmann, D. J. Arndt-Jovin, and T. M. Jovin, “Fluorescence lifetime imaging in an optically sectioning programmable array microscope (PAM),” Cytometry A 67(2), 112–118 (2005).
[Crossref] [PubMed]

Artal, P.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

Atchison, D. A.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

Baghaie, A.

A. E. Salmon, R. F. Cooper, C. S. Langlo, A. Baghaie, A. Dubra, and J. Carroll, “An Automated Reference Frame Selection (ARFS) Algorithm for Cone Imaging with Adaptive Optics Scanning Light Ophthalmoscopy,” Transl. Vis. Sci. Technol. 6(2), 9 (2017).
[Crossref] [PubMed]

Bedggood, P.

P. Bedggood and A. Metha, “Optical imaging of human cone photoreceptors directly following the capture of light,” PLoS One 8(11), e79251 (2013).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Variability in bleach kinetics and amount of photopigment between individual foveal cones,” Invest. Ophthalmol. Vis. Sci. 53(7), 3673–3681 (2012).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Direct visualization and characterization of erythrocyte flow in human retinal capillaries,” Biomed. Opt. Express 3(12), 3264–3277 (2012).
[Crossref] [PubMed]

Bedggood, P. A.

A. Duan, P. A. Bedggood, A. B. Metha, and B. V. Bui, “Reactivity in the human retinal microvasculature measured during acute gas breathing provocations,” Sci. Rep. 7(1), 2113 (2017).
[Crossref] [PubMed]

A. Duan, P. A. Bedggood, B. V. Bui, and A. B. Metha, “Evidence of Flicker-Induced Functional Hyperaemia in the Smallest Vessels of the Human Retinal Blood Supply,” PLoS One 11(9), e0162621 (2016).
[Crossref] [PubMed]

Bigelow, C. E.

D. X. Hammer, R. D. Ferguson, T. E. Ustun, C. E. Bigelow, N. V. Iftimia, and R. H. Webb, “Line-scanning laser ophthalmoscope,” J. Biomed. Opt. 11(4), 041126 (2006).
[Crossref] [PubMed]

Bird, A. C.

E. Y. Chew, T. E. Clemons, T. Peto, F. B. Sallo, A. Ingerman, W. Tao, L. Singerman, S. D. Schwartz, N. S. Peachey, and A. C. Bird, “Ciliary neurotrophic factor for macular telangiectasia type 2: results from a phase 1 safety trial,” Am. J. Ophthalmol. 159(4), 659–666 (2015).
[Crossref] [PubMed]

Blanco, E. R.

T. Zhang, P. Godara, E. R. Blanco, R. L. Griffin, X. Wang, C. A. Curcio, and Y. Zhang, “Variability in Human Cone Topography Assessed by Adaptive Optics Scanning Laser Ophthalmoscopy,” Am. J. Ophthalmol. 160(2), 290–300 (2015).
[Crossref] [PubMed]

Botelho, J. V.

J. C. Horton, A. B. Parker, J. V. Botelho, and J. L. Duncan, “Spontaneous Regeneration of Human Photoreceptor Outer Segments,” Sci. Rep. 5(1), 12364 (2015).
[Crossref] [PubMed]

Bui, B. V.

A. Duan, P. A. Bedggood, A. B. Metha, and B. V. Bui, “Reactivity in the human retinal microvasculature measured during acute gas breathing provocations,” Sci. Rep. 7(1), 2113 (2017).
[Crossref] [PubMed]

A. Duan, P. A. Bedggood, B. V. Bui, and A. B. Metha, “Evidence of Flicker-Induced Functional Hyperaemia in the Smallest Vessels of the Human Retinal Blood Supply,” PLoS One 11(9), e0162621 (2016).
[Crossref] [PubMed]

Burns, S. A.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

A. E. Elsner, T. Y. Chui, L. Feng, H. X. Song, J. A. Papay, and S. A. Burns, “Distribution differences of macular cones measured by AOSLO: Variation in slope from fovea to periphery more pronounced than differences in total cones,” Vision Res. 132, 62–68 (2017).
[Crossref] [PubMed]

L. Sawides, A. de Castro, and S. A. Burns, “The organization of the cone photoreceptor mosaic measured in the living human retina,” Vision Res. 132, 34–44 (2017).
[Crossref] [PubMed]

J. Lammer, S. G. Prager, M. C. Cheney, A. Ahmed, S. H. Radwan, S. A. Burns, P. S. Silva, and J. K. Sun, “Cone Photoreceptor Irregularity on Adaptive Optics Scanning Laser Ophthalmoscopy Correlates With Severity of Diabetic Retinopathy and Macular Edema,” Invest. Ophthalmol. Vis. Sci. 57(15), 6624–6632 (2016).
[Crossref] [PubMed]

A. de Castro, G. Huang, L. Sawides, T. Luo, and S. A. Burns, “Rapid high resolution imaging with a dual-channel scanning technique,” Opt. Lett. 41(8), 1881–1884 (2016).
[Crossref] [PubMed]

S. A. Burns, R. Tumbar, A. E. Elsner, D. Ferguson, and D. X. Hammer, “Large-field-of-view, modular, stabilized, adaptive-optics-based scanning laser ophthalmoscope,” J. Opt. Soc. Am. A 24(5), 1313–1326 (2007).
[Crossref] [PubMed]

Campbell, M.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

A. Roorda, F. Romero-Borja, W. Donnelly III, H. Queener, T. Hebert, and M. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10(9), 405–412 (2002).
[Crossref] [PubMed]

Carroll, J.

A. E. Salmon, R. F. Cooper, C. S. Langlo, A. Baghaie, A. Dubra, and J. Carroll, “An Automated Reference Frame Selection (ARFS) Algorithm for Cone Imaging with Adaptive Optics Scanning Light Ophthalmoscopy,” Transl. Vis. Sci. Technol. 6(2), 9 (2017).
[Crossref] [PubMed]

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

M. A. Wilk, A. M. Dubis, R. F. Cooper, P. Summerfelt, A. Dubra, and J. Carroll, “Assessing the spatial relationship between fixation and foveal specializations,” Vision Res. 132, 53–61 (2017).
[Crossref] [PubMed]

P. Tanna, M. Kasilian, R. Strauss, J. Tee, A. Kalitzeos, S. Tarima, A. Visotcky, A. Dubra, J. Carroll, and M. Michaelides, “Reliability and Repeatability of Cone Density Measurements in Patients With Stargardt Disease and RPGR-Associated Retinopathy,” Invest. Ophthalmol. Vis. Sci. 58(9), 3608–3615 (2017).
[Crossref] [PubMed]

R. F. Cooper, M. A. Wilk, S. Tarima, and J. Carroll, “Evaluating Descriptive Metrics of the Human Cone Mosaic,” Invest. Ophthalmol. Vis. Sci. 57(7), 2992–3001 (2016).
[Crossref] [PubMed]

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual Foveal Cone Structure in CNGB3-Associated Achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

R. F. Cooper, Y. N. Sulai, A. M. Dubis, T. Y. Chui, R. B. Rosen, M. Michaelides, A. Dubra, and J. Carroll, “Effects of Intraframe Distortion on Measures of Cone Mosaic Geometry from Adaptive Optics Scanning Light Ophthalmoscopy,” Transl. Vis. Sci. Technol. 5(1), 10 (2016).
[Crossref] [PubMed]

B. S. Liu, S. Tarima, A. Visotcky, A. Pechauer, R. F. Cooper, L. Landsem, M. A. Wilk, P. Godara, V. Makhijani, Y. N. Sulai, N. Syed, G. Yasumura, A. K. Garg, M. E. Pennesi, B. J. Lujan, A. Dubra, J. L. Duncan, and J. Carroll, “The reliability of parafoveal cone density measurements,” Br. J. Ophthalmol. 98(8), 1126–1131 (2014).
[Crossref] [PubMed]

J. Carroll, D. B. Kay, D. Scoles, A. Dubra, and M. Lombardo, “Adaptive optics retinal imaging--clinical opportunities and challenges,” Curr. Eye Res. 38(7), 709–721 (2013).
[Crossref] [PubMed]

P. Godara, A. M. Dubis, A. Roorda, J. L. Duncan, and J. Carroll, “Adaptive optics retinal imaging: emerging clinical applications,” Optom. Vis. Sci. 87(12), 930–941 (2010).
[Crossref] [PubMed]

J. Rha, B. Schroeder, P. Godara, and J. Carroll, “Variable optical activation of human cone photoreceptors visualized using a short coherence light source,” Opt. Lett. 34(24), 3782–3784 (2009).
[Crossref] [PubMed]

Cepko, C. L.

C. L. Cepko, “Emerging gene therapies for retinal degenerations,” J. Neurosci. 32(19), 6415–6420 (2012).
[Crossref] [PubMed]

Chen, D. C.

Chen, F. K.

M. N. Muthiah, C. Gias, F. K. Chen, J. Zhong, Z. McClelland, F. B. Sallo, T. Peto, P. J. Coffey, and L. da Cruz, “Cone photoreceptor definition on adaptive optics retinal imaging,” Br. J. Ophthalmol. 98(8), 1073–1079 (2014).
[Crossref] [PubMed]

Chen, L.

Cheney, M. C.

J. Lammer, S. G. Prager, M. C. Cheney, A. Ahmed, S. H. Radwan, S. A. Burns, P. S. Silva, and J. K. Sun, “Cone Photoreceptor Irregularity on Adaptive Optics Scanning Laser Ophthalmoscopy Correlates With Severity of Diabetic Retinopathy and Macular Edema,” Invest. Ophthalmol. Vis. Sci. 57(15), 6624–6632 (2016).
[Crossref] [PubMed]

Chew, E. Y.

E. Y. Chew, T. E. Clemons, T. Peto, F. B. Sallo, A. Ingerman, W. Tao, L. Singerman, S. D. Schwartz, N. S. Peachey, and A. C. Bird, “Ciliary neurotrophic factor for macular telangiectasia type 2: results from a phase 1 safety trial,” Am. J. Ophthalmol. 159(4), 659–666 (2015).
[Crossref] [PubMed]

Chiang, J.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual Foveal Cone Structure in CNGB3-Associated Achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Choi, S. S.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref] [PubMed]

Chui, T. Y.

A. E. Elsner, T. Y. Chui, L. Feng, H. X. Song, J. A. Papay, and S. A. Burns, “Distribution differences of macular cones measured by AOSLO: Variation in slope from fovea to periphery more pronounced than differences in total cones,” Vision Res. 132, 62–68 (2017).
[Crossref] [PubMed]

R. F. Cooper, Y. N. Sulai, A. M. Dubis, T. Y. Chui, R. B. Rosen, M. Michaelides, A. Dubra, and J. Carroll, “Effects of Intraframe Distortion on Measures of Cone Mosaic Geometry from Adaptive Optics Scanning Light Ophthalmoscopy,” Transl. Vis. Sci. Technol. 5(1), 10 (2016).
[Crossref] [PubMed]

Chulay, J. D.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual Foveal Cone Structure in CNGB3-Associated Achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Chung, M.

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.) 25(3), 301–308 (2011).
[Crossref] [PubMed]

Clemons, T. E.

E. Y. Chew, T. E. Clemons, T. Peto, F. B. Sallo, A. Ingerman, W. Tao, L. Singerman, S. D. Schwartz, N. S. Peachey, and A. C. Bird, “Ciliary neurotrophic factor for macular telangiectasia type 2: results from a phase 1 safety trial,” Am. J. Ophthalmol. 159(4), 659–666 (2015).
[Crossref] [PubMed]

Coffey, P. J.

M. N. Muthiah, C. Gias, F. K. Chen, J. Zhong, Z. McClelland, F. B. Sallo, T. Peto, P. J. Coffey, and L. da Cruz, “Cone photoreceptor definition on adaptive optics retinal imaging,” Br. J. Ophthalmol. 98(8), 1073–1079 (2014).
[Crossref] [PubMed]

Coletta, N. J.

Collier, R.

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Supplementary Material (5)

NameDescription
» Visualization 1       Retinal image acquired without anamorphic detection
» Visualization 2       Retinal image acquired with anamorphic detection
» Visualization 3       Retinal image acquired at the fovea
» Visualization 4       Retinal image acquired at the eccentricity of 1.8° nasally
» Visualization 5       Retinal image acquired at the eccentricity of 5° nasally

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Figures (9)

Fig. 1
Fig. 1 The incompatibility between adequate digitization of optical resolution and light collection efficiency in a line-scan ophthalmoscope and proposed solution. (a) A diagram of image formation in a line-scan ophthalmoscope. The retinal structure illuminated by the light line is imaged by a line camera. (b) The Airy disk, i.e., the point spread function (PSF), formed by the imaging system on the line imaging chip of the camera. To ensure sufficient digitization of the optical resolution, the PSF must be sampled by 4.88 × 4.88 pixels [57]. Under this condition, a line imaging chip can only collect a small portion of the PSF, resulting in significant imaging light loss and poor image signal to noise ratio. (c) When the PSF is focused within one pixel, the optical resolution is digitized insufficiently. (d) As a technical solution, the PSF of is designed with an elliptic form instead of a circular one.
Fig. 2
Fig. 2 The DMD based high speed AO ophthalmoscope with anamorphic imaging. The Top row shows the anamorphic PSF of the system across the imaging field (left edge, middle, and right edge). The ellipses indicate diffraction limited PSF. SLD: Superluminescent diode. DMD: Digital micromirror device. CL0-CL2: Cylindrical lens. DF: Dichroic filter. BS1, BS2: Beam splitters. L0-L4: Lenses. S1-S6: Spherical mirrors. GS: Galvanometric scanner. FM: Flat mirrors. WS: Wavefront sensor. DM: Deformable mirror. The top right part of the light delivery box shows configurations of DMD. The “on” and “off” states of the micromirrors are represented by solid and hollow squares, respectively [56]. The Light collection module shows the elliptic PSF formed by anamorphic imaging on the image chip of the line camera (spL2048-140km, Basler Co., Germany).
Fig. 3
Fig. 3 Improvement of brightness and definition of retinal imaging by anamorphic detection. (a) A single frame of retinal image acquired without anamorphic detection (see Visualization 1 for the video). (b) A single frame taken at the same retinal location with anamorphic detection (see Visualization 2 for the video). (c) The corresponding normalized histograms of retinal images taken without and with anamorphic detection. The histogram of the image acquired without anamorphic detection is truncated due to insufficient photons. The images were acquired at the eccentricity of 0.8° nasally. The images size is about 300 µm on a side. All images were taken at 200 FPS.
Fig. 4
Fig. 4 Lateral resolution. (a) The USAF target image was acquired with DMD ‘all on’ configuration. (b) The cross-section profiles of the horizontal and vertical lines marked with yellow lines in (a). (c) The USAF target image was acquired with DMD ‘2 × 2 on’ configuration. (d) The cross-section profiles of horizontal and vertical lines marked with yellow lines in (c). H: horizontal. V: vertical.
Fig. 5
Fig. 5 Axial resolution. (a) Axial resolution measured with DMD static and dynamic modulation. The configuration that η = 2 indicates that each microreflector consists of 2 × 2 DMD micromirrors. δ/η is the spatial duty cycle of the modulation. The setting that η = 2 and δ/η = 1 (the brown line with crosses) is essentially the static DMD ‘2 × 2 on’ state. Data measured in the DMD ‘all on’ setting are plotted for comparison (the blue line with diamonds). (b) Axial resolution measured in dynamic DMD modulation with different microreflector configurations. The configuration that η = 1 indicates that each microreflector consists of 1 DMD micromirror. The axial resolution measured in the ‘DMD all on’ setting (red asterisk) is drawn for comparison.
Fig. 6
Fig. 6 Photoreceptor and retinal capillary imaging. (a) Retinal image acquired at the fovea (see Visualization 3). (b) Retinal image acquired at the eccentricity of 1.8° nasally (see Visualization 4). All cells are cone photoreceptors. Images in (a) and (b) are in linear grey scale. (c) Retinal image acquired at the eccentricity of 5° nasally, revealing cones (larger and brighter dots) and surrounding rods (smaller dots). The image is in logarithmic scale (see Visualization 5, raw video is in linear grey scale). All images were taken from an eye of a subject with normal retinal health, and registered from a set of 100 successive frames. (d) - (f) Retinal capillaries imaged at different depths. The numbers on top right corners of the panels indicate the imaging light defocus power (in diopter: D) induced by the deformable mirror while AO was correcting the ocular wave aberration. Zero D corresponds to the plane of the inner segment layer of the cone photoreceptors. The capillaries were extracted using the standard deviation of a sequence of 50 successive images [50]. All images were acquired with a frame rate of 200 FPS. Scale bars represent 50 μm.
Fig. 7
Fig. 7 The repeatability of cone mosaic metrics assessed in images acquired with different frame rate at 1° eccentricity nasally (Subject 1). (a), (b), and (c) are Voronoi diagrams of the ROI in images acquired at 100 FPS, 200 FPS, and 800 FPS, respectively. Blue Voronoi cells are 6-sides, and red ones are not. (d) Cone density (CD) repeatability under different frame rates. (e) Percentage of six-sided cells (PSSC) repeatability. (f) Intercellular distance (ICD) repeatability. (g) Nearest neighbor distance (NND) repeatability. (h) Nearest neighbor regularity (NNR) repeatability. (i) Voronoi cell area regularity (VCAR) repeatability. Error bars indicate 1 standard deviation (SD). Numbers above the bars are the coefficients of variation (CV) from 12 series measurement of this metric.
Fig. 8
Fig. 8 The repeatability of cone mosaic metrics assessed in images acquired with different frame rate at 1° eccentricity nasally (Subject 2). (a), (b), and (c) are Voronoi diagrams of the ROI in images acquired at 100 FPS, 200 FPS, and 800 FPS, respectively. Blue Voronoi cells are 6-sides, and red ones are not. (d) Cone density (CD) repeatability under different frame rates. (e) Percentage of six-sided cells (PSSC) repeatability. (f) Intercellular distance (ICD) repeatability. (g) Nearest neighbor distance (NND) repeatability. (h) Nearest neighbor regularity (NNR) repeatability. (i) Voronoi cell area regularity (VCAR) repeatability. Error bars indicate 1 standard deviation (SD). Numbers above the bars are the coefficients of variation from 12 series measurement of this metric.
Fig. 9
Fig. 9 The repeatability of cone mosaic metrics assessed in images acquired with different frame rate at 2° eccentricity nasally (Subject 1). (a), (b), and (c) are Voronoi diagrams of the ROI in images acquired at 100 FPS, 200 FPS, and 800 FPS, respectively. Blue Voronoi cells are 6-sides, and red ones are not. (d) Cone density (CD) repeatability under different frame rates. (e) Percentage of six-sided cells (PSSC) repeatability. (f) Intercellular distance (ICD) repeatability. (g) Nearest neighbor distance (NND) repeatability. (h) Nearest neighbor regularity (NNR) repeatability. (i) Voronoi cell area regularity (VCAR) repeatability. Error bars indicate 1 standard deviation (SD). Numbers above the bars are the coefficients of variation (CV) from 12 series measurement of this metric.

Metrics